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ORIGINAL RESEARCHpublished: 18 December 2020

doi: 10.3389/fmars.2020.601277

Edited by:Aldo S. Pacheco,

National University of San Marcos,Peru

Reviewed by:Laura J. May-Collado,

University of Vermont, United StatesArtur Andriolo,

Juiz de Fora Federal University, Brazil

*Correspondence:Arielle M. Amrein

arielleamrein@gmail.com

Specialty section:This article was submitted to

Marine Megafauna,a section of the journal

Frontiers in Marine Science

Received: 31 August 2020Accepted: 23 November 2020Published: 18 December 2020

Citation:Amrein AM, Guzman HM,

Surrey KC, Polidoro B and Gerber LR(2020) Impacts of Whale Watching on

the Behavior of Humpback Whales(Megaptera novaeangliae)

in the Coast of Panama.Front. Mar. Sci. 7:601277.

doi: 10.3389/fmars.2020.601277

Impacts of Whale Watching on theBehavior of Humpback Whales(Megaptera novaeangliae) in theCoast of PanamaArielle M. Amrein1,2* , Hector M. Guzman3, Katie C. Surrey1,2, Beth Polidoro1,2,4 andLeah R. Gerber1,2

1 School of Life Sciences, Arizona State University, Tempe, AZ, United States, 2 Center for Biodiversity Outcomes, ArizonaState University, Tempe, AZ, United States, 3 Smithsonian Tropical Research Institute, Panama City, Panama, 4 Schoolof Mathematics and Natural Sciences, Arizona State University, Tempe, AZ, United States

Ecotourism focused on whales and dolphins has become a popular activity and animportant source of revenue for many countries. Whale watching is vital to supportingconservation efforts and provides numerous benefits to local communities includingeducational opportunities and job creation. However, the sustainability of whale-basedecotourism depends on the behavior and health of whale populations and it is crucialthat ecotourism industries consider the impact of their activities on whale behavior.To address this statement, we collected behavioral data (e.g., change in swimmingdirection, frequency of breaching, slap behaviors, diving, and spy hops) from humpbackwhales (Megaptera novaeangliae) in the marine protected area of Las Perlas Archipelagooff the Pacific coast of Panama. The goal was to determine if tourist vessel presencehad an influence on whale behaviors. We conducted this study during the humpbackwhale breeding season from August through September 2019. Based on 47 behavioralobservations, we found that higher boat density corresponded with humpback whales’frequency of direction changes, which based on previous literature is believed to be asign of disturbance. Alternatively, no changes in behavior were observed with varyingboat density. This result is important given Panamanian regulations first implementedin 2007 by Resolution AMD/ARAP No. 01, 2007 prohibit whale-based tourism fromdisturbing whales, which is explicitly measured by changes in whale behavior. Becausethere is no systematic monitoring of whale watching activity to enforce the regulations,there is currently little compliance from tour operators and tourists. The integration ofanimal behavior research into management planning should result in more effectiveregulation and compliance of such conservation policies.

Keywords: ecotourism, Megaptera novaeangliae, disturbance, stress, behavioral ecology, animal welfare,wildlife-ecotourism

INTRODUCTION

Wildlife-based ecotourism, which includes whale watching, is identified as, “tourism basedon encounters with non-domesticated animals. . .[which] can occur in either an animal’snatural environment or in captivity” (Higginbottom, 2004). It provides economic benefits tomany countries around the world (Hoyt, 2001; O’Connor et al., 2009; Guidino et al., 2020;

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Wiener et al., 2020) and has increased drastically in popularityover the past 50 years. Globally, over 13 million tourists taketrips to view cetaceans each year, generating over $2 billion USdollars in revenue across 119 countries (Hoyt and Hvenegaard,2002; O’Connor et al., 2009; Stoeckl et al., 2010; Guidinoet al., 2020; Wiener et al., 2020). Whale watching industries arerapidly growing in developing countries such as Cambodia, Laos,Nicaragua, and Panama (Hoyt, 2001; O’Connor et al., 2009).While ecotourism activities have many economical, educational,and ecological benefits relating to conservation, there have beenmany published studies that conversely question the benefitsof this form of ecotourism, proposing that these activities maybe harming the wildlife involved (Parsons, 2012; Leslie et al.,2015; Larson et al., 2016). Therefore, these activities deservea higher level of scrutiny and monitoring to ensure theirongoing sustainability and economic, community, educational,etc., contributions (Stamation et al., 2007; The InternationalEcotourism Society, 2015).

The main contribution of whale watching is that it providesa stable financial alternative to the traditionally consumptiveuse of whales through hunting or “whaling.” The growinginflux of tourists coming to watch whales provides the revenuerequired to support local communities and cultures whilesimultaneously supporting whale conservation efforts (Wearinget al., 2014). Whale watching focused on humpback whales(Megaptera novaeangliae) was also found to be effective inencouraging natural resource protection and patronization oflocal businesses, especially when tour guides take care todisseminate conservation messages to tourists (Peake et al., 2009).In addition, through specific platforms such as whale watching,the public has the opportunity to come in contact with oftenendangered or threatened wildlife and learn about conservationefforts (García-Cegarra and Pacheco, 2017). This practice fallsunder “responsible” whale watching guidelines, which is definedas an environmental and economical use of whales that issustainable, promotes whale conservation, and education whilesimultaneously supporting local communities (O’Connor et al.,2009). This is especially relevant given that the rapid urbanizationof society is prompting people to desire opportunities to“reconnect” themselves with nature (Curtin and Kragh, 2014).

The growing popularity of this industry also has drawbacksespecially in developing countries, where regulatory frameworksare often lacking leading to a higher likelihood that animalwelfare and safety regulations will be ignored (Sitar et al.,2016; Kassamali-Fox et al., 2020). Tour boat operators mayintentionally or inadvertently utilize locations that experiencelittle enforcement or actively violate the rules of responsiblewhale watching in the desire to attract more clients, ultimatelyleading to detrimental impacts on whale welfare (Corbelli, 2006;Parsons, 2012; Kessler and Harcourt, 2013; Sitar et al., 2016).Accordingly, the International Whaling Commission (IWC)established measures to protect whales and published guidelinesfor responsible whale watching in 1997 (International WhalingCommission, 1997). Unfortunately, with little enforcementin some countries, there are still high levels of detrimentalwhale interactions with non-consumptive whale-watching vessels(Parsons, 2012).

During encounters when high numbers of vessels are present,whales will often exhibit a high frequency of behavioral shifts,such as direction changes, which are reflective of avoidance tacticsemployed when whales encounter predators (Frid and Dill, 2002;Williams et al., 2002). These behaviors, combined with the high-speeds and unpredictable approach angles often displayed byvessels, greatly increase the risk of collision (Guzman et al.,2013). In addition, whales must expend extra energy to avoidboats, while decreasing the occurrence of necessary survivalactivities (e.g., nursing, foraging, and reproduction; Morete et al.,2007; Stamation et al., 2010; Schaffar et al., 2013; Fournet et al.,2018; Fiori et al., 2019). This is especially true in breedingareas that are primarily frequented by mother and calf groupsbecause they are more susceptible to whale watching disturbances(Morete et al., 2007; García-Cegarra et al., 2019). One studysuggested that long-term disruption of routine behaviors causedby high levels of negative boat and whale interactions could havelasting reproductive impacts on humpback whale populations(Braithwaite et al., 2015), while others highlight potential impactsdue to the inability for whales to effectively communicate dueto “acoustic masking” from loud boat sounds (Rossi-Santos,2016; Erbe et al., 2018, p. 290). This could result in reducedsuccess when finding a mate in breeding areas, locating foodin feeding areas, and further expended energy to increase callvolume or duration (Foote et al., 2004; Fournet et al., 2018;Putland et al., 2018).

Given these issues and mediating factors, the marine andcoastal areas of Panama are ideal locations for observing thewhale–vessel interactions and potential repercussions. Panama isa popular tourist destination due to the presence of the PanamaCanal, which only serves to increase daily levels of vessel trafficthrough its service as an important commercial trade route.Humpback whales from the southeast Pacific population migratefrom their feeding grounds in Chile and Antarctica to the tropicalareas along the Pacific coasts of Central America for the breedingseason (Rasmussen et al., 2007; Acevedo et al., 2017). The seasonextends from June to October, and sometimes December, withpeaks in August and September (Guzman et al., 2015). Thehumpback whale population of this archipelago is estimatedto be around 1,000 individuals, with about 25–50 calves bornannually (Guzman et al., 2015). This population of humpbackwhales is identified as Breeding Stock G (International WhalingCommission, 1998), which is one of the seven “stocks” inhabitingoceans in the southern hemisphere. This specific populationundertakes one of the longest migration distances (Stone et al.,1990; Acevedo et al., 2017) of more than 16,000 km roundtripfrom the feeding grounds to the breeding grounds (Rasmussenet al., 2007; Félix and Guzmán, 2014; De Weerdt et al., 2020),with the entire stock swimming along 9,000 km of coastline (Félixet al., 2011). Female and calf pairs tend to remain closer to shore(Glockner and Venus, 1983; Bruce et al., 2014; Oña et al., 2017)while adults prefer more direct routes in deeper waters (Félix andHaase, 2005; Rasmussen et al., 2012; Félix and Guzmán, 2014;Guzman and Félix, 2017). Mother–calf pair preference for coastalwaters poses higher risks of vessel collision and entanglement ingillnets, as fishermen and commercial ships share these waters(Félix and Guzmán, 2014). Although whales are migratory for

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the majority of the year, they congregate in waters less than200 m deep for their annual breeding season. Hence, the shallowwaters of the Pacific of Panama are ideal for mother humpbackwhales giving birth, due to the lack of competitive males pursuingthe females, ocean turbulence, and predators (Flórez-Gonzálezet al., 1994; Corkeron and Connor, 1999; Darling and Nicklin,2002; Cartwright and Sullivan, 2009; Craig et al., 2014; Pitmanet al., 2015). The objective of this study is to determine if tourboat number and mode of approach to whales elicit changesin their behavior frequencies in the Las Perlas Archipelago inPanama. We hypothesize that whales will decrease the frequencyof certain behaviors as indicators of disturbance when boatpresence increases and when boat captains are not complyingwith regulations.

MATERIALS AND METHODS

Study SiteThis study was conducted in the Las Perlas Archipelago (8.41◦N,79.02◦W) in the Gulf of Panama, which lies about 60 kmsoutheast of Panama City (Figure 1). The archipelago comprises250 basaltic rock islands and islets spread over 1,688 km,making it the fourth-largest coastal marine protected area ofPanama (ADM/ARAP No. 1 from 13 February 2007; Guzmanet al., 2008). We recorded behavioral responses of humpbackwhales in the Las Perlas Archipelago between 18 August and 6September 2019, with observational sessions consisting of bothland-based and boat-based visual behavioral studies, from alookout point on Contadora Island (the largest inhabited island)and a ∼9.75 m whale-watching vessel, respectively. 720 totalminutes were recorded, with 135 min from land-based surveysand 585 min from boat-based surveys, throughout the 16 days ofresearch. Our boat, unlike other boats, took extreme precautionsto minimize our potential disturbance to the whales by followingthe mandated regulations such as keeping a 250 m distance,having a certified boat operator with a permit for commercialoperations, and limiting observation times to 30 min per group.

Data were collected using a whale group-follow protocol, asthe presence of competitive groups (i.e., a female surroundedby one or several males displaying active behaviors, such asbreaching, striking, charging, and trumpeting), made it difficultto follow specific individuals (Mann, 1999). Therefore, a focalfollow method was used. Variables in the data included fourgroup types (e.g., competitive, mother–calf pair and escort,pair, and lone whale), group size, behaviors (see Table 1),Global Positioning System (GPS) coordinates, whale directionchanges, and the number of boats within approximately 300 mof the whales. The distance was visually measured for both boatand land surveys by the researcher using Chapera island as areferential point. We then estimated how far the whale wasbetween the boat or Contadora (the lookout point) and Chapera.Diving behavior was measured by the number of fluke dives thatoccurred within 15 min by a focal whale (including adults andcalves). Other recorded variables were measured to characterizethe environmental conditions during the survey which includedthe Beaufort wind scale and cloud cover (Spencer et al., 2006).

Description of Group TypesA mother and calf pair consisted of a large whale (assumed tobe the mother) together with a small individual one-third thelength of the adult, the calf (Chittleborough, 1958; Cartwrightand Sullivan, 2009). A lone whale was a single individual travelingwithout any other individuals observed within 50 m, while pairscontained two adult whales traveling in the same direction.Meanwhile, whales were considered a group (or “pod”) if three ormore individuals were moving in the same direction and less than50 m from each other. These groups were considered competitiveif three or more adult humpback whales were within 50 m ofeach other, exhibiting high energy behavior. The compositionof these groups usually consisted of a single female (with orwithout calf), with one or more males that are showing a highfrequency of surface behavior and physical contact with eachother (Herman et al., 2007).

Behavior FrequencyDuring boat-based surveys, observation began once humpbackwhales were spotted within 300 m of the research vessel, whichgave a clear view for researchers to collect data. Land-based studysessions began once a whale was spotted within approximately3 miles (4.8 km) of the lookout point given the increased visibilityand the use of Outland X 10x42 binoculars. For both landand boat surveys, once whales were spotted, one researchertracked the GPS coordination and direction change of humpbackwhales. The GPS coordinates were subjectively estimated bythe researcher judging the whale’s distance between the twoislands of Contadora (the lookout point) and the island ofChapera in viewpoint of the land-based studies. Researcherspinpointed the estimated location of the whale on the device’smap using a mobile device’s GPS application and recorded thecoordinates. A change in direction was visually measured byconsidering the location and forward positioning of whales whensurfacing. If the whale group surfaced in a different locationand in a different facing direction than their original position,it indicated a direction change. The second researcher trackedall 15 behaviors from Table 1 as well as group type, groupsize, Beaufort wind scale, number of boats, and cloud cover. Ifmore than one group was spotted during a study session, thegroup closest to the observer was tracked. Studies occurred ingood weather conditions (Beaufort wind scale < 5) but wereobstructed in severe weather conditions (Beaufort scale > 5;Cloud cover = 100%), if whale sightings were lost, or if the whalegroup split during the observation session. If a whale or pod werespotted, then every 15 min, observations of weather conditions,and a scan of behaviors (e.g., scan sample) were conducted andthen recorded. We did not record the frequency of behaviors thatoccurred continuously over 15 min.

While counting the number of vessels, boats were onlyincluded in a session if it was observed to be clearly followingthe humpback whale group and if they were within 300 mof the whale. Observation sessions that included zero boatspresent were considered controls. Since the lack of boat presenceserved as the control variable, these observations could onlybe conducted during land-based studies to avoid inadvertent

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FIGURE 1 | Map showing the study area in Las Perlas archipelago in Panama. The solid lines indicate the limits of the protected area. The shaded area is the core ofthe fieldwork and data collection, but qualitative observations extended to the outer areas.

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TABLE 1 | Description of behavior categories for humpback whale behaviors(based on descriptions by: Glockner-Ferrari and Ferrari (1984) and Gabriele (1992)(adapted from Bauer, 1986; Helweg, 1989; Corkeron, 1995; Darling and Nicklin,2002).

Behavior name Description

Breach Whale leaps out of the water, spinning in the air beforere-entering

*Tail-Up Dive Whale lifts tail out of the water and attains a vertical anglefor deep dives

Peduncle Arch Whale arches its back showing the dorsal fin that usuallyoccurs after they surface to breathe

Head Raise/SpyHop

Raises head vertically out of the water while stationary,flippers outstretched

*Pectoral Fin Slap Slaps flipper down onto the surface of the water

*Tail Slap Raises flukes out of the water and slaps them on thesurface

*Side Fluke Swimming on one side with one fluke extending above thesurface

*Head Slap Jumps out of the water and hits the ventral side of headforcefully on surface

*Chase/Charge Lunges at another whale, often bubble-streaming

*Strike Intentionally hits another whale with fluke extending abovethe surface

Collide Whales collide, appears to be intentional

Trumpet Extended low-trumpet or “foghorn-like” sound from theblowhole

Singing An extended high-pitched sound made by male humpbackwhales

Resting Motionless movement in which whale stays in one place

*Avoidance The rapid change in direction to avoid a potential threat

* indicates behaviors which are characteristic of avoidance or stress.

effects from the research vessel. Many behavioral events, suchas singing, trumpeting, side flukes, and colliding, were omittedfrom the study given their low or absent sample sizes. Otherswere combined into a single category because of low individualincidence. For example, head slaps, tail slaps, and pectoral finslaps were all combined into “slap behaviors.”

Statistical AnalysisWe used a Chi-squared goodness of fit test to measure theinfluence of boat density on whale behavior. We used this methoddue to its established ability to test the relationship betweenbehaviors and boat presence (Bagdonavicius and Nikulin,2011). To normalize the data, we proportionally measured thebehavioral observations using a linear regression hypothesis test.Individual whales may express different behavioral responseswhen faced with a disturbance. Thus, to determine if grouptype was a significant predictor of a whale’s behavior, weapplied a Kruskal–Wallis and a post hoc pairwise Wilcoxontest to assess which sets of groups had a significantly differentnumber of direction changes from each other (Pohlert, 2014).Results are reported as mean ± standard error followed bythe p-value. Finally, we used a regression model featuring aPearson’s product-moment test to test the strength or weaknessbetween the relationship between direction changes and thenumber of vessels. Such a test is essential for drawing a best-fit

line through the two variables (direction change and vesselnumbers) and examining how far off the variables are from theregression line (Benesty et al., 2009). Both boat and land-basedstudies were included in every analytical test. We performed allstatistical analyses in R version 3.6.0 (R Core Team, 2017) andMicrosoft Excel (2003).

RESULTS

Between August and September 2019, we recorded 47 behavioralsessions. Groups with mother and calf pairs and mother–calfand escort groups were pooled for analysis due to the lowsample size of mother–calf and escort groups (three groupstotal). These 47 samples consisted of 24 mother and calf pairsand escort sightings (51%), 11 competitive group sightings(23%), seven lone whale sightings (15%), and five paired adultsightings (11%). The average number of individuals in a podwas 2.57 with a range of one individual to a maximum ofeight individual whales in the study. Thereafter, we comparedthe explanatory variable (number of boats) and two dependentvariables (direction change and behavior). Mother–calf andescort pods made up 50% of the samples involving boats but wererarely observed during controlled samples, making up only 14%of the data, respectively.

Behavior State TransitionsWe collected behavioral observations in both the absenceand presence of vessels. Overall, the Chi-squared goodness offit test indicated a significant difference among all behaviors(X2 = 57.1147, p < 0.001). In the presence of vessels, breachinggradually increased as boat numbers grew, then significantlydeclined with more than three boats present (2%; Figure 2). Thisdecline in breaching often occurred when boats were chasingwhales. Humpback whales were most often seen executing slapbehaviors (e.g., pectoral fin slaps, tail slaps, and head slaps)during sampling with zero boats present (55%). Alternatively, thefrequency of diving behavior (e.g., tail up-dives) varied widelyamong different levels of boat presence (36% of dives occurred insessions with two boats, 29% with four or more boats, 28% withzero boats, 5% with one boat, and 2% with three boats), but therewas no discernable pattern related to the number of vessels. Whilespy hops/head rises were rarely seen, they only occurred duringsituations when boats were present.

More than 62% of behaviors were observed in elevencompetitive groups ranging from three to eight individuals withineach pod. Mother–calf and escort groups provided 20% of thebehavioral data samples, five pair groups provided 16%, andseven lone whale samples accounted for only 2% of the behavioraldata. Breaching was the only behavior that was not predominatelyexpressed by competitive whale groups. Competitive groupsmade up 23% of the breaching while other non-competitivegroups made up the other 77%. This occurred primarily withpaired groups (40%), followed by mother–calf and escort pods(36%) and lone whales (<2%). In addition, a linear regressionmodel (Figure 3) capturing the proportion of behavioraltransitions presented no clear indication of significance of change

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FIGURE 2 | Megaptera novaeangliae. Total number of categorized whale behavior occurrences observed during varying boat presence while conductinggroup-follow behavioral samples.

FIGURE 3 | The frequency of behavioral observations as a proportion of the total numbers of observations for each boat type.

with varying boat numbers (Breach: R2 = 0.42, p > 0.05; Dive:R2 = 0.09, p > 0.05; Slap: R2 = 0.13, p > 0.05; Spy hop: R2 = 0.34,p > 0.05).

Direction Change and Group TypeWe conducted a post hoc pairwise Wilcoxon test (Figure 4) toassess which group types exhibited a significantly different

number of direction changes from each other. Of thecomparisons across all whale group types, the pair versuscompetitive group type and pair versus calf group typewere the only pairwise comparisons rejected (Z = 1.68,16 ± 0.474, p < 0.05; Z = 1.68, 29 ± 0.486, p < 0.05,respectively). The rest of the pair-wise comparisons, therefore,supported the null hypothesis, which assumes little to no

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FIGURE 4 | Megaptera novaeangliae. Box plot comparing the number of direction changes of four different whale group types (competitive groups, lone groups, calfgroups, and pairs). Groups with shared letters are not significantly different.

difference occurred among the number of direction changes foreach group type.

Relationship of Direction Change toNumber of VesselsAs the number of vessels during an observational sessionincreased, the number of whale direction changes increased.Using a linear regression model, direction change, and thenumber of vessels also produced a positive relationship(R2 = 0.38, p < 0.001; Figure 5). Few direction changes occurredwhen zero boats were present, with only one competitivegroup changing direction (once) during a controlled observation.However, the number of observations within each treatmentwas unequal. Observation sessions with one boat occurred mostfrequently (34%) followed by four or more boats (22%), zeroboats (20%), two boats (15%), and three boats (9%). Mother–calfand escort groups had the most amount of direction changes,with 26 total direction alterations (see Figure 5). This resultmay be attributed to calf-mother-escort groups being the mostobserved group type (51% of samples).

DISCUSSION

Behavior FrequencyThe number of boats present had varying effects on the fourbehavior events measured during our study: breaching, diving,slap behaviors, and spy hop. It is theorized that breaching

represents a communicative tactic caused by whales slappingtheir bodies on the surface when vocalization is obstructed(Whitehead, 1985; Dunlop et al., 2010; Kavanagh et al., 2017).While numerous factors can hinder vocalization such as highwind speeds, rain, and vessel noise, whale communication in thisenvironment could have been blocked by higher levels of vesselnoise, leading to an increase in the observed breaching behavior(Whitehead, 1985; Richardson et al., 1995; Moore et al., 2012;Cholewiak et al., 2018; Gabriele et al., 2018).

This is reflected in the results as the increase in vessel numberappeared to be associated with higher incidences of breaching.

FIGURE 5 | Megaptera novaeangliae. Observed correlation between thenumber of boats and the total number of direction changes while conductinggroup-follow behavioral samples.

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However, the breaching frequency decreased once vessel numbersexceeded two boats. It is also possible that crowding frommultiple boats limited surface area, restricting available space forwhales to breach. Whale breaching has also been theorized to bea form of play, especially when exhibited by calves (Whitehead,1985), which could explain the relatively high involvement ofcalf pairs in breaching. Alternatively, breaching may also be atactic for male humpback whales to display their physical abilitieswhen seeking a mate, which explains the high breach count thatalso occurred in pairs and competitive groups (Whitehead, 1985;Darling and Nicklin, 2002; Pacheco et al., 2013). Unfortunately,due to boats being more inclined to violate the existing whale-watching regulations, the high levels of whale-chasing exhibitedby vessels could negatively influence the stress level of the whales,reducing their breaching. These behaviors could eventually bereplaced with an increase in avoidance behaviors, such asdirection change and longer dive times (Stamation et al., 2010).

The number of slap behaviors increased when the numberof boats declined. This observation supports the theory thatif a whale is close to another group, they will communicatethrough slapping behavior (Shapiro, 2008). Whales of both sexesslap their fins to communicate or gain attention when seekinga mate. Females specifically use this slapping tactic since theydo not sing (Deakos, 2002; Herman et al., 2007). This behaviorwas especially evident in this study as Panama is a hotspot forbreeding humpback whales, with increased competitive behaviorsexhibited between males and females.

Competitive groups had the highest incidences for three ofthe four observed behaviors: slap behaviors, spy hopping, anddiving. However, these results may differ from other studiesconducted at different times of the year because whale behaviorchanges dramatically during breeding seasons (Corkeron, 1995;Stamation et al., 2010; Schaffar et al., 2013).

Tail slaps are the most common surface behavior observed,most likely because they are not associated with high energeticcosts (Noren et al., 2009; Segre et al., 2020). Therefore, humpbackwhales may only resort to breaching when noise pollution (suchas that caused by high vessel presence) increases, as the soundof breaching travels much farther than the noise of a tail orpectoral fin slap. Schuler et al. (2019) attribute the change insurface behavior to the disparity between the weight and surfacearea of a whale’s tail versus that of their body. Researchers ofprevious studies also found an increase in vessel number to causehumpback whales exhibiting surface behaviors to switch fromsurface activity to traveling. This may have long-term effects onindividuals and groups because of the high energy expenditure ofreacting to the boats (Schuler et al., 2019; Table 2).

Spy hops or head raises occurred less frequently than the otherdocumented behaviors, but more occurred during sessions ofhigh boat presence. This could suggest that spy hops ensue whenwhales wish to view activities above the surface (Galvin, 2006).In this study, as spy-hopping only occurred when vessels werepresent, the whales were most likely curious about the vesselsfollowing them, thereby supporting this hypothesis.

The linear regression model displayed no clear indication ofdifferent behavior event frequencies when correlated with varyingvessel numbers. This result could be an indication of habituation

TABLE 2 | Categories of behaviors used in this study from prior studies on theimpacts of whale watching on orcas and humpback whale behavior.

Behaviorsstudied

Findings References

Avoidancebehaviors

Cetaceans increased their path sinuosity butdecreased the linearity of their path with vesselspresent.

Senigagliaet al., 2016

Avoidancebehaviors

Humpback whales showed avoidancebehaviors 84% of the time, increasing thesinuosity of path and change in direction withincreased vessel approach.

Schaffaret al., 2013

Group type andbehavior

Humpback whale calf pods were much morereactive to vessels than non-calf pods anddisplayed more avoidance behaviors whenvessels came within 100 meters of the whale.

Stamationet al., 2010

Behavior Humpback whales that engaged in surfaceactivity were likely to switch behavior whenvessel presence increased. Long-term effectsare associated with the loss of energy whenwhales react to boats.

Schuler et al.,2019

Behavior Blue whales showed fewer foraging behaviorsthe closer vessels approached them, leading toa reduction in energy for foraging which couldhave long-term effects on Blue whales.

Guilpin et al.,2020

Behavior Humpback whales exhibited more surfacebehaviors with increased vessel exposure,which could lead to energetic consequences.

Di Clementeet al., 2018

to anthropogenic presence and noise, which poses additionalrisks (Richardson et al., 1995; Stone and Yoshinaga, 2000), aswell as the range of different types of vessels which vary in theiracoustic volume. With Panama being one of the central ports inthe global cargo-shipping network, higher levels of vessel trafficwill likely only increase the risk of whale-vessel collision (Kaluzaet al., 2010; Guzman et al., 2013). While the risk of collision withlarger ships has been reduced due to the passage of the Gulfof Panama Traffic Separation Scheme in 2014 (CITE), the lackof regulation enforcement among non-commercial ships meanspotentially hazardous collisions between cetaceans and vessels(Panama Maritime Authority, 2014).

This is an observational study and we did not experimentallymanipulate boat numbers. Thus, the number of samples differsbetween boat numbers. Further studies are required to confirmif humpback whales in the Las Perlas Archipelago display thesame behavioral responses that whale groups exhibit in publishedstudies (Darling and Nicklin, 2002; Williams et al., 2002; Lusseauand Bejder, 2007; Morete et al., 2007; Stamation et al., 2010;Schaffar et al., 2013; Fiori et al., 2019; Schuler et al., 2019).

Direction Change and Group TypeWe suggest that the whale group type was not a significantpredictor of the number of direction changes exhibited. Thesignificant difference between pairs versus competitive groupsand pairs versus groups found in Las Perlas Archipelago maybe the result of competitive groups being in a setting wherethey must be vigilant and always watching their competitors;however, this attentive attribute may cause them to exhibit stress-based behaviors to avoid boats. The concern of energy costs

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is especially relevant with regard to calf groups since it seemswhale watching vessels prefer following calf groups due to theirplayful behavior. As calves may feel more threatened by boatsthan other group types, Panamanian regulations have extra lawsto protect calves, given their vulnerable state. We saw a significantdifference even with a small sample size, but a greater number ofsamples would clarify the extent of the relationship. Nevertheless,these results support findings from previous whale behavioralreports. In one study, group type was included as an explanatoryvariable to predict dive time, swim speed, and directness indexand found the relationship between group type and the othervariables had no significance and did not lead to a better fittingmodel (Schaffar et al., 2013). Unfortunately, we were unable tomeasure changes in swim speed in this study. Another studyfound pods with calves exhibit higher levels of activity comparedto non-calf pods (Stamation et al., 2010). This supports the resultsof our study, which showed groups with calves executing thelargest number of direction changes. However, due to the smallsample size of this study, no other conclusions can be confidentlyderived regarding whether whale behavior can be predicted by thewhale group type.

Relationship of Direction Change toNumber of VesselsThe results of this study displayed a positive correlation betweenthe direction change and the number of vessels present, withmost of these changes being exhibited by pod groups containingcalves (Figure 5). Calves are especially vulnerable to increasedvessel presence due to the higher likelihood of vessel collision,less knowledge of vessel movement, and decreased ability topartake in essential behaviors such as feeding, nursing, andlearning how to care for themselves (Scheidat et al., 2004;Stamation et al., 2010). This may explain why calf groupshad the highest sum of direction changes compared to allother whale pod types since vessels had a higher preferencefor chasing whale groups with calves. Results from this studyshow clear indications of behavioral change being a consequenceof increased vessel presence, violating Panama’s regulation thatprohibits vessels from “chang[ing] the behavior of cetaceans”(sensu Carlson, 2010).

Previous research suggests that the proximity of boats is arobust predictor of the number of directional changes a whalemight exhibit (Schaffar et al., 2013). As direction change is a tactichumpback whales use to avoid predators, this avoidance behaviormay also be utilized when faced with a boat, which could beviewed as a perceived threat (Schaffar et al., 2013; Table 2). Severalresearchers suggest direction changes are also related to stressand could indicate an increased level of physiological disturbance(Kruse, 1991; Beale, 2007; Schaffar et al., 2013; Schuler et al.,2019; see Table 2). Thus, while avoidance behavior may ensureself and group preservation, it also comes at a physiologicalcost to the organism. Not only can increased levels of stressnegatively impact an organism’s health, but it can also inhibitnormal whale behavior and interactions, which can disruptsocial interactions (mother–calf pair in particular), mating, andforaging (Beale, 2007; Lusseau et al., 2009).

Regulatory Implications and ComplianceDue to concerns about whale interactions with vessels, Panamainitially passed Resolution Decree ADM/ARAP No. 1 on 13February 2007, to control the level of vessel disturbance oncetaceans to conserve their populations. Regulations from thisdecree require operators to have a permit for commercialoperations, have a maximum of two whale-watching vesselsper group, take extra care when calves are present, maintain a250 m distance from the whales, and limited observation timesto 30 min per group or no more than 15 min when calves areinvolved, and obey the restriction of individuals from entering thewater with whales, to prevent altering the behaviors of cetaceans(sensu Carlson, 2010).

Lack of enforcement from the Panamanian government haselicited the reiteration and repeated implementation of thesepolicies every year. While boat operators may be aware of thepolicies currently in place, there is little structural enforcementto ensure regulatory compliance. Better enforcement protocolsmust, therefore, be enacted to better ensure vessels are abidingby Panama’s regulations. To reduce vessels from violating whalewatching regulations, a satellite-based monitoring system shouldbe implemented to track the activities of these vessels. Thistechnology has already been shown to be successful in fisheriesmanagement plans and has alleviated illegal, unreported, andunregulated (IUU) fishing (Schmidt, 2005). Alternatively, lack ofcompliance may also be the result of poor communication fromthe government concerning the regulations, leaving local whalewatching companies and boat operators with a lack of knowledgeabout the existence of these laws (Sitar et al., 2016, 2017).

In summary, Panama has strict whale watching operationregulations that are not being followed or enforced in the LasPerlas Archipelago. At multiple times throughout this study,we observed all laws pertaining to vessel regulations beingbroken at least once by boats. The on-going lack of regulationenforcement may result in more audacious decisions from boatoperators in the future, leading to harmful or even lethalcollisions with adult whales and calves. At the very least,these results show increased changes in whale behavior whenvessels are present, which is illegal according to Panamanianprotocols (sensu Carlson, 2010). Thus, it is highly recommendedthat both boat operators and tourists be educated aboutregulations and the importance of abiding by the law. Whilethe purpose of this study was not to propose the eradicationof whale watching, it was to highlight the potential harm beingdone due to the lack of compliance with responsible whalewatching protocols. Responsible whale watching develops aninterdependent relationship between people and whales: peoplegain from the ecosystem services provided by whales andeconomic income from this tourism industry, while whalesbenefit from less stress from vessels and indirectly from tourguides expanding environmental awareness and enlighteningtourists about environmental or conservation issues. Continuedwhale research, monitoring, and modeling efforts in Panamamust be implemented to better inform management decisionsregarding stricter regulatory and enforcement protocols that arevital to minimize disturbance on this vulnerable population ofhumpback whales.

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Conclusion and Future ResearchRecommendationsAlthough our study is limited to the short-term impacts ofboat vessel presence on humpback whale behavior, long-termchanges in behavior may indirectly lower reproduction rates(Lusseau and Bejder, 2007). This can occur through drownedout vocalizations and a reduction in the success of whalesfinding mates due to vessels altering whale group dynamicsand travel direction (Weilgart, 2013). Additionally, whale healthcan be negatively affected due to chronic levels of stress,increases in energy expenditures, and discontinuation of essentialbehaviors such as feeding, resting, nursing, etc. (Parsons, 2012).Constant changes in behavior and less concentration on survivalactivities could result in eventual population declines over time,as groups with calves are the most vulnerable, especially aswhale watching vessels prefer following calf groups for theircharismatic physical characteristics and playful behaviors. Dueto this increased vulnerability, Panamanian regulations need tocontain extra provisions to ensure the protection of whale calves(sensu Carlson, 2010).

However, behavior and stress may not necessarily be coupledin a way that can be easily observed. This was evident inthis study when some whales did not appear to change theirbehaviors despite increased levels of vessel interaction. It has beenproven that animals may not exhibit avoidance behaviors, butnevertheless experience high levels of stress hormones (Schuleret al., 2019). For this reason, additional physiological studiesare recommended. Previous studies have shown that biopsysamples of cortisol found within blubber samples can providemeasurements of stress levels over several weeks to a month,which would provide insight into how stress levels may fluctuatethroughout an entire whale watching season as the number oftourist boats changes (Noren and Mocklin, 2012; Teerlink et al.,2018). Alternative cortisol collection methods including fecal(Wasser et al., 2000; Rolland et al., 2005; Hunt et al., 2006; Burgesset al., 2013) and blowhole spray have also been shown to providemore acute measurements of stress related to vessel presence.

Future behavioral research should also include the use ofmore accurate measuring methods and tools. For example,the use of a theodolite tool would produce accurate distancemeasurements between vessels and whales, which is essential forunderstanding if distance impacts whale behaviors. Unmannedaerial systems (UAS) (drones) would allow for the collection ofmore accurate behavioral samples via less invasive observationalmethods (Torres et al., 2018). Visual observations could also bemaintained more consistently by drones due to optimal viewingangles, as traditional vessel-based observations can only be madewhile the whale is surfacing. Additional social surveys should becollected from tourists, local communities, and boat operatorsto help us understand their impression of the whale watchingindustry and whether whale watching is, generally, of value.

In Las Perlas Archipelago, whale watching generates incomefor local communities. It also creates employment opportunitiesand provides ecosystem services to tourists, residents, and boatoperators. However, if disturbances to these whales continueunabated, it may lead to the eventual abandonment of the

Archipelago by the population, as has occurred in other popularwhale-watching locations elsewhere in the world (Dean et al.,1985). The satisfaction of tourists is vital to the ongoingsustainability of the Panamanian ecotourism industry, as a reportby the World Bank in 2005 found that two-thirds of all visitors toPanama were motivated to visit the country due to environmentalor ecotourism reasons and income from international touriststotaled 7% of the GDP (World Bank, 2005, p. 9). Decreases intourist motivation to partake in ecotourism activities such aswhale watching potentially cause the industry to suffer, therebyaffecting the Panamanian economy. This is already somewhatevidenced by the drastic decrease in tourism caused by theCOVID-19 pandemic. Understanding the dynamic changes inhuman well-being and animal population viability are critical forestablishing effective wildlife conservation strategies. Variationsin socioeconomic factors that benefit the local communities canmotivate more people to protect and care about whales. It istherefore important to consider the coupled nature of ecologicaland socio-economic systems to understand the impacts of wildlifetourism on both humans and nature.

DATA AVAILABILITY STATEMENT

The raw data supporting the conclusions of this article will bemade available by the authors, without undue reservation.

ETHICS STATEMENT

The animal study was reviewed and approved by SmithsonianTropical Research Institute and the Institutional Animal Careand Use Committee.

AUTHOR CONTRIBUTIONS

AA is the primary author and this research is a component ofher M.S. thesis paper. HG, BP, KS, and LG contributed to theoverall idea, writing, research, data collection, and analysis of thispaper. All authors contributed to the article and approved thesubmitted version.

FUNDING

Funding for this project was provided by the partnershipbetween Arizona State University and the Smithsonian TropicalResearch Institute.

ACKNOWLEDGMENTS

Special thanks to our funders, research assistants, reviewers,boat captains, and colleagues that supported and refined ourresearch and writing. We thank the government of Panama forsupport and providing the research permit SE/A-79-18 from theMinisterio de Ambiente.

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Conflict of Interest: The authors declare that the research was conducted in theabsence of any commercial or financial relationships that could be construed as apotential conflict of interest.

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